Hatching Asynchrony Reduces the Duration, Not the Magnitude, of Peak Load in Breeding Green-Rumped Parrotlets (Forpus Passerinus)

Behav Ecol Sociobiol (1999) 45: 444±450 Ó Springer-Verlag 1999

ORIGINAL ARTICLE

Rodney B. Siegel á Wesley W. Weathers Steven R. Beissinger Hatching asynchrony reduces the duration, not the magnitude, of peak load in breeding green-rumped parrotlets (Forpus passerinus)

Received: 16 July 1998 / Accepted after revision: 13 December 1998

Abstract The peak load reduction hypothesis suggests parrots, raptors, herons, and passerines. Numerous ex- that hatching asynchrony in altricial birds is adaptive planations of the proximate causes and adaptive value of because it reduces parental workload during the most asynchronous hatching have been proposed, including energetically costly time in brood rearing. By staggering 17 distinct hypotheses, many of which may operate in the ages of their ospring, parents may ensure that all concert with one another (Clark and Wilson 1981; nestlings do not reach maximum energy demand Magrath 1990; Stoleson and Beissinger 1995). The peak simultaneously. To test the hypothesis, we used the load reduction hypothesis (Hussell 1972) suggests that doubly labeled water technique to measure the energy parents may lessen their workload at the most energet- expenditure of green-rumped parrotlets (Forpus passer- ically demanding time in brood rearing by staggering the inus) that reared experimentally manipulated synchro- ages of their young, so that all nestlings do not reach nous and asynchronous broods. Peak metabolic rates of maximum energy demand at the same time. the two experimental groups did not dier, but parents Mathematical simulations have tested the peak load of asynchronous broods metabolized signi®cantly less reduction hypothesis without actually creating or ob- energy than did parents of synchronous broods serving synchronous broods. Bryant and Gardiner throughout the ®rst half of the brood-rearing period. (1979) predicted synchronous hatching would increase Our results suggest that hatching asynchrony in par- peak brood energy demand by 7±8% in house martins rotlets substantially shortens the temporal duration of (Delichon urbica), but Lessells and Avery (1989) calcu- high brood energy demand, but does not reduce the lated that synchronous hatching in European bee-eaters magnitude of peak energy demand. (Merops apiaster) would increase parents' provisioning rate by only 1%. Mock and Shwagmeyer (1990) mod- Key words Asynchronous hatching á Peak load á eled the eects of synchronous and asynchronous Forpus passerinus á Green-rumped parrotlets á hatching on parental eort under a variety of clutch Doubly labeled water sizes and hatching intervals. They concluded that peak load reduction seldom approaches 5% under natural scenarios and is unlikely to provide substantial selection pressure for asynchronous hatching. Introduction Experimental studies have only sometimes demon- strated increased indicators of nestling food demand in Hatching asynchrony is widespread among altricial synchronous compared to asynchronous broods. Syn- birds, occurring across a diversity of groups including chronous hatching increased nestling food consumption throughout the brood-rearing period in American kes- R.B. Siegel (&)1 á Wesley W. Weathers trels (Falco sparverius) and cattle egrets (Bubulcus ibis), Department of Avian Sciences, University of California apparently due to increased sibling competition (Fujioka Davis, CA 95616-8532, USA 1985; Mock and Ploger 1987; Wiebe and Bortoletti S.R. Beissinger 1994). In other species, synchronous hatching aected Department of Environmental Science, Policy and Management neither parental mass loss during the breeding season University of California, Berkeley, CA 94720-3110, USA (Amundsen and Slagsvold 1991) nor provisioning rate Present address: (HeÂ bert and Barclay 1986; Slagsvold 1997; Stoleson and 1The Institute for Bird Populations, P.O. Box 1346 Point Reyes Station, CA 94956-1346, USA Beissinger 1997). e-mail: [email protected], Tel.: +1-415-663-2051 Green-rumped parrotlets (Forpus passerinus) are Fax: +1-415-663-9482 among the most likely of species to reduce peak load 445 energy demands through asynchronous hatching be- grassland and scattered clumps of small trees and palms, is de- cause broods are large and hatch unusually asynchro- scribed in detail by Troth (1979) and O'Connell (1989). Nestboxes are described in Beissinger and Bucher (1992). nously over periods of up to 2 weeks (Beissinger and Green-rumped parrotlets are small (24±36 g), mostly granivor- Waltman 1991; Mock and Schwagmeyer 1990). Yet ex- ous parrots native to grasslands and forest edges of northern South perimentally induced synchronous hatching in parrotlets America (Forshaw 1989). Clutch size averages seven eggs, which is increased nestling survival without aecting nest provi- unusually large for a tropical bird (Beissinger and Waltman 1991). sioning rate (Stoleson and Beissinger 1997), suggesting Females generally lay eggs at 1- to 2-day intervals and begin incubation after laying the ®rst egg. The resulting hatching spread of that hatching asynchrony does not reduce peak load. up to 2 weeks is among the largest of any species studied and leads Similar provisioning rates or mass changes in parents to dramatic size disparities among nestmates (Beissinger and rearing synchronous and asynchronous broods may not Waltman 1991; Stoleson and Beissinger 1997). First-hatched chicks be strong enough evidence to refute the peak load re- may complete nearly half their 4- to 5-week period in the nest before their youngest sibling hatches. duction hypothesis. Provisioning rate and mass change Females are fed by their mates while they incubate their eggs are only indices of parental eort, not direct measures and brood young nestlings, but they switch from primarily (Siegel et al., in press). Provisioning rate may not be brooding to primarily foraging and provisioning nestlings 1± sensitive enough to detect subtle but nonetheless im- 2 weeks after the ®rst chick hatches. Chicks ¯edge 28±35 days after hatching, and post-¯edging parental care appears to be minimal portant dierences in parental eort, particularly if the (Waltman and Beissinger 1992; Stoleson and Beissinger 1997). quantity of food delivered varies substantially between nest visits, or if the energy expenditure necessary to gather a constant quantity of food varies considerably Measuring parent ®eld metabolic rate (FMR) over time. Parental mass change is an even less reliable index of parental eort, as mass change and daily energy We checked nestboxes daily to ascertain laying dates of all eggs. expenditure correlate positively in some species studied, After females stopped laying, but before eggs hatched, we trans- ferred eggs among nests to create clutches of eight eggs. Clutches but negatively or not at all in others (Bryant 1988). either hatched asynchronously, mimicking the natural hatching In contrast with provisioning rate and mass change, pattern (10±12 days between the ®rst and last egg), or synchro- the doubly labeled water technique (DLW) measures nously (within 3 days). We chose a clutch size slightly larger than directly the energy expenditure of free-living animals the modal clutch size, hypothesizing that any elevation of parental workload due to synchronous hatching would be greatest (and (Lifson and McClintock 1966). In this study, we used most likely to be measurable) in large broods. Perfect synchrony DLW to test directly for the ®rst time whether asyn- could not be achieved because incubation periods of individual eggs chronous hatching reduces peak parental energy varied slightly. All manipulated clutches received eggs from mul- expenditure. We measured energy expenditure of green- tiple donor nests, and procedures for moving eggs followed those rumped parrotlets rearing experimentally manipulated used by Stoleson and Beissinger (1997). Daily checks of nestboxes when hatching became imminent synchronous and asynchronous broods early, midway assured certainty of hatching dates. To maintain broods of eight through, and late in the brood-rearing period. We ®rst nestlings, we replaced eggs that failed to hatch, and nestlings that measured parents' energy expenditure 5 days after their died due to predation or other causes, with similar-aged eggs or ®rst chick hatched, when synchronous broods were fully nestlings from other nests. Partial brood loss occurred in about one-fourth of nests, and chicks were usually less than 5 days old hatched but only about half of the chicks in asynchro- when they died. Parents readily accepted and fed substitute nes- nous broods had hatched. We measured energy expen- tlings. We excluded broods from the remainder of the experiment if diture again 11 days later, after all chicks in both they were missing more than one nestling and appropriately aged experimental treatments had hatched, and then a third replacement nestlings were unavailable. We used the single-sample DLW protocol to measure the FMR time on day 27, just before the ®rst-hatched chick of parents at 5, 16 and 27 days after their ®rst chick hatched. The ¯edged. We predicted that synchronous broods would single-sample protocol is less invasive than the more frequently have greater energy demands than asynchronous broods used double-sample method, and has been shown to yield accept- on each sampling day, and parents rearing synchronous able accuracy; Webster and Weathers (1989) provide a detailed broods would consequently expend more energy than exploration of potential errors associated with the single-sample method. Parent birds were mist-netted or captured inside their parents rearing asynchronous broods. We expected that nestbox, injected intramuscularly with isotopically labeled water energy expenditure of parents, regardless of experimen- and released in their nestbox. Prior to release, we held 16 of the tal treatment, would be greatest around day 27, but that birds for 1 h for isotope equilibration and subsequent blood sam- parents rearing asynchronous broods would have sub- pling to estimate total body water. We attempted to recapture all birds approximately 24 or 48 h after release, and collect blood from stantially lower peak energy expenditures. the brachial vein. Actual intervals between injection and bleeding ( SD) averaged 23.6 3.5 h for birds recaptured 1 day after injection, and 49.1 7.8 h for birds recaptured after 2 days. Blood samples were refrigerated and then distilled to obtain pure Methods water (Nagy 1983; Wood et al. 1975). Water samples were assayed for tritium activity (Searle model Mark III liquid scintillation counter, toluene-Triton X100-PPO scintillation cocktail) and for Study area and species oxgen-18 content by cyclotron-generated proton activation of oxygen-18 to ¯uorine-18 with subsequent counting of the positron- In 1995 and 1996, we studied color-banded green-rumped parrot- emitting ¯ourine-18 in a Packard Gamma-Rotomatic counting lets breeding in PVC-pipe nestboxes at Hato Masaguaral, an active system (Wood et al. 1975). Body water volumes and rates of car- cattle ranch in the state of GuaÂ rico in the Venezuelan llanos bon dioxide production were calculated using the equations of (8°31¢N, 67°35¢W). The ranch, characterized by seasonally ¯ooded Nagy (1980, 1983). 446

Data were analyzed using SYSTAT (Wilkinson 1990) and SAS (1988). We con®rmed homogeneity of variance of FMR measurements (Bartlett's test: B = 1.2, P = 0.30) and used analysis of variance (ANOVA) to assess the eects of sex, brood age, and synchrony treatment on parent FMR. We used one-tailed t-tests to assess the prediction that asynchronous hatching would reduce parent energy expenditure on each sampling day.

Results

We successfully measured FMR of at least one parent on at least one sampling day at 25 synchronous nests and 22 asynchronous nests. At many nests, we measured parent FMR on multiple sampling days. To account for any resulting pseudoreplication, we included `individual,' nested within sex, as an eect in the ANOVA. Sex and number of days since the ®rst chick hatched signi®cantly aected parent FMR, and the overall eect of synchrony treatment was nearly signi®cant (Table 1). Energy savings due to hatching asynchrony were apparent for both males and females on each sampling day (Fig. 1), though not all dierences were statistically signi®cant. By day 5, all eight eggs in synchronous clutches had already hatched, whereas only two to four eggs had hatched in asynchronous nests. As a result day 5 FMRs of both males and females tending asynchronous broods averaged about 17% lower than rates of their counterparts rearing completely hatched synchronous broods. Females' FMRs were lower because they generally spent day 5 brooding chicks and incubating remaining eggs, while males were foraging and deliver- Fig. 1 Average ®eld metabolic rate (FMR) of female (a)andmale(b) ing food to their nestlings and mates. Hatching asyn- green-rumped parrotlets tending experimentally created synchronous chrony signi®cantly reduced FMR on day 5 among both and asynchronous broods of eight nestlings. Shown are males and females (Table 2). By day 16, all eight eggs in means 1 SE, with number of parents tending synchronous broods indicated above the curves, and number of parents tending both synchronous and asynchronous clutches had hat- asynchronous broods indicated below the curves ched. FMRs of parents rearing asynchronous broods averaged 13% lower than those of their counterparts rearing synchronous broods. Despite relatively small signi®cant for males (Table 2). FMRs of parents rearing sample sizes, this reduction in FMR due to hatching synchronous and asynchronous broods did not signi®- asynchrony was signi®cant for females and was nearly cantly dier on day 27, but our sample sizes were small (Table 2). Day-27 FMRs did not dier signi®cantly by sex (t-tests: t 0.7, df 11, P 0.47 for synchronous Table 1 ANOVA testing eects of days since the ®rst chick hat- parents; t 1.1. df 8, P 0.30 for asynchronous ched (5, 16 or 27), sex, and synchrony treatment (synchronous or asynchronous) on ®eld metabolic rate measurements of breeding green-rumped parrotlets Table 2 Percentage decrease in average ®eld metabolic rates of green-rumped parrotlets tending synchronous versus asynchronous Eect df FPbroods 5, 16, and 27 days after their ®rst chick hatched (t-tests are one-tailed) Days since ®rst 2 13.4 <0.001 chick hatched Day Percent tdfP Sex 1 19.0 <0.001 decrease Synchrony treatment 1 3.9 0.06 Days ´ sex 2 1.2 0.32 Males Days ´ synchrony 2 1.0 0.37 5 17.0 3.4 23 <0.01 treatment 16 12.5 1.6 18 0.06 Sex ´ synchrony 1 0.0 0.93 27 2.8 0.2 8 0.41 treatment Females Sex ´ days ´ treatment 2 0.6 0.54 5 16.9 2.4 35 <0.05 Individual (sex) 80 0.8 0.79 16 12.9 2.0 21 <0.05 Error 36 27 5.1 0.6 11 0.27 447 parents), so we pooled values from both sexes to provide Stoleson and Beissinger (1997; unpublished data) greater statistical power. With the sexes pooled, FMRs monitored ¯edging interval (the time from hatching to of parents rearing asynchronous brood were still not ¯edging) and growth of 337 green-rumped parrotlet signi®cantly lower than FMRs of parents rearing syn- chicks reared in synchronous or asynchronous broods, chronous broods (t 1.1, df 21, P 0.27). By day 27, and described growth rate using the logistic equation. FMRs of parents rearing synchronous and asynchro- They found that ¯edging interval and growth rate both nous broods had converged for both males and females, varied with hatching order and synchrony treatment at the time when energetic demands of the brood were (Stoleson and Beissinger 1997). We used their average likely greatest. growth rates and ¯edging intervals, partitioned by hatching order and synchrony treatment, to generate growth curves for each nestling in a hypothetical asynchronous brood of eight nestlings hatching over 11 days Discussion and a hypothetical synchronous brood of eight nestlings hatching over 3 days. We estimated resting metabolic Hatching asynchrony did not signi®cantly reduce par- rates (kJ/day) of growing nestlings throughout the nes- ents' peak energy expenditure. We expected the total tling period from nestling mass, using Eq. 7 of Weathers energy demand of natural broods to peak around day and Siegel (1995), which provides a phylogenetically 27, because ®rst-hatched nestlings begin ¯edging at day robust estimate of the resting metabolism of altricial 28. On day 27, male and female parents of asynchronous nestlings. broods metabolized only 2.8% and 5.1% less energy, Summing nestling energy demands yielded estimates respectively, than did their synchronous counterparts. of the energy required for resting metabolism in syn- Such modest reductions in peak load are consistent with chronous and asynchronous broods on each day from the predictions of the model of Mock and Schwagmeyer ®rst hatching to last ¯edging (Fig. 2a). Cumulative (1990). They suggest that even species with unusually large clutches and long laying intervals, such as parrotlets, would be unlikely to reduce peak energy demands substantially through asynchronous hatching. Parents rearing asynchronous broods achieved greater energy savings earlier in the brood-rearing period (Ta- ble 2), as we predicted. Relative energy savings were greatest at day 5, when many of the asynchronous chicks had not hatched but parents at synchronous nests tended fully hatched broods. In absolute terms, parents at this early stage of brood rearing were working well below the highest observed rate of energy expenditure (Fig. 1), whether their broods were synchronous or asynchronous. At day 16, energy savings due to hatching asynchrony were substantial (statistically signi®cant for females, and very nearly so for males), and parents, especially of synchronous broods, were working much closer to apparent peak load levels. Males and females rearing asynchronous broods metabolized, 85% and 79%, respectively, as much energy on day 16 as on day 27, compared with 94% and 86% in males and females rearing synchronous broods. Asynchronous hatching thus reduced the temporal duration of high parental energy expenditure, rather than the magnitude of the energy expenditure on a single day of peak parental eort. The energy expenditure of parents likely re¯ects the food requirements of their broods. However, even large changes in parental eort may result in only minor changes in parent FMR, because parent FMR includes not just energy expended on parental care, but also non-reproductive components of the energy budget. We estimated the energy demand of synchronous and asynchronous broods throughout the nestling period to see if the consequences of asynchronous hatching on Fig. 2 Estimated energy required by synchronous and asynchronous brood energy demand could explain the shortened broods of eight nestlings for resting metabolism (a) and resting period of high parental energy expenditure. metabolism plus growth (b) 448 resting metabolism requirements for synchronous and The brood energy demand models in Fig. 2b account asynchronous broods were nearly identical (5137 kJ for resting metabolism and growth, but they do not in- for synchronous broods, 5252 kJ for asynchronous clude energy necessary for thermoregulation or activity, broods). Hatching asynchrony reduced brood maxi- which together may account for as much as one-third of mum daily energy requirement for resting metabolism cumulative metabolizable energy in growing nestlings by only 2%, which could explain why asynchrony (Drent et al. 1992). If cumulative thermoregulatory and had no signi®cant eect on peak parent FMR. Such a activity costs of nestling parrotlets are concentrated late minor reduction in peak energy requirement is unlikely in the nestling phase, a reasonable supposition, then to provide selection pressure for asynchronous total brood energy requirements, even for synchronous hatching. broods, could still peak around day 30. The discrepancy The overall shapes of the two brood energy demand between the shape of the synchronous-brood energy curves in Fig. 2a dier much more than do their max- demand curve in Fig. 2b and the empirical FMR mea- ima. The energy demand of the asynchronous brood surements, however, suggests that activity and thermo- increases slowly at ®rst and then rises steeply to a peak regulatory costs may dier between synchronous and of 227 kJ/day on day 31. In contrast, the resting energy asynchronous broods. requirement of the synchronous brood increases rapidly Energy demand curves for nestling thermoregulation early in brood rearing, and then plateaus near the peak and activity are dicult to predict, but there are nu- load of 232 kJ/day. Parents of asynchronous broods merous reasons why they could dier markedly between must supply their nestlings with enough food to meet a synchronous and asynchronous broods. If synchronous resting requirement of 227 kJ/day on a single peak load hatching alters female brooding behavior, nest thermal day, whereas parents of synchronous broods must sup- environments could dier substantially, resulting in ply at least that much energy for 7 days to meet the dierent thermoregulatory costs for chicks in synchro- energy demand of their chicks. Similarly, the asynchronous and asynchronous broods. Even without dieren- nous brood requires 204 kJ/day, or 90% of its peak ces in brooding behavior, detailed studies of nestbox energy demand for resting metabolism, for 6 consecutive microclimate are needed to determine if the presence of days, whereas the synchronous brood requires at least many similar-aged large nestlings substantially warms that much energy for 14 days. the nest, and perhaps alters thermoregulatory costs. Our estimates of energy demand for brood resting Activity costs may also dier between synchronous and metabolism suggest that temporal variation in brood asynchronous broods. Asynchronous hatching may energy demand explains why asynchronous hatching avoid extra energy expenditure due to competition for shortens the duration of high parent FMR without food, either by imposing a stable dominance hierarchy substantially reducing the magnitude of peak FMR. on the brood (Hahn 1981), or by enabling parents to However, resting metabolism constitutes only around preferentially feed younger nestlings, and thereby dis- half of total chick energy demand (Drent et al. 1992). To courage an escalation of energetically costly begging produce a more complete approximation of brood en- (Stamps et al. 1985). Such energy savings seem unlikely ergy demand, we added estimates of the energy content in green-rumped parrotlets because nestlings do not of accumulated tissue (RE, estimated by Eq. 13.10 of engage in ®ghts and parents have diculty successfully Weathers 1996) to our estimates of nestling resting me- seeking out and feeding youngest chicks in asynchro- tabolism. Although incorporating RE into the models nous broods (Stoleson and Beissinger 1997). Further- substantially altered the shape of the synchronous-brood more, recent evidence suggests that begging may only energy demand curve (Fig. 2b), hatching asynchrony account for a trivial portion of nestling energy budgets still considerably reduced the duration of high brood (Chappell and Bachman, in press; McCarty 1996). energy demand. Brood energy requirements for resting Although our brood energy demand estimates have metabolism plus RE peaked at 258 kJ/day in the syn- limited predictive power because of their incomplete- chronous brood and at 248 kJ/day in the asynchronous ness, they demonstrate the potential for asynchronous brood, yielding a peak load reduction of about 4%. hatching to change the distribution of parental eort While the asynchronous brood requires 248 kJ/day on a required throughout the brood-rearing period. With or single day of peak demand, the synchronous brood re- without accounting for RE, our energy demand esti- quires at least that much energy for 8 consecutive days. mates suggest that asynchronous hatching substantially Similarly, the asynchronous brood requires 223 kJ/day, reduces the duration of high brood energy demand, or 90% of its peak demand, for 10 days, whereas the without markedly aecting the magnitude of peak en- synchronous brood needs at least that much energy for ergy demand. Models or empirical tests of the peak load 20 consecutive days. reduction hypothesis that narrowly focus on a single day The energy demand of the asynchronous brood of peak energy demand will fail to discern such dier- (Fig. 2b) remained maximal at day 31, but the energy ences. Our results also highlight the potential limitations demand of the synchronous brood peaked much earlier of relying on provisioning rate as an index of parental in the season, at day 17. This result is inconsistent with eort, rather than constructing more complete time parent FMRs, which were higher on day 27 than on day budgets, or directly measuring FMR. Provisioning rate 16, irrespective of synchrony treatment. in parrotlets does not vary with synchrony treatment 449

(Stoleson and Beissinger 1997), yet our FMR data show Chappell MA, Bachman GC (in press) The exercise capacity of that asynchronous hatching alters the temporal distri- house wren nestlings: begging chicks are not working as hard as they can. Auk bution of parental energy expenditure. Clark AB, Wilson DS (1981) Avian breeding adaptations: hatching Reduced FMRs of parents rearing asynchronous asynchrony, brood reduction, and nest failure. Q Rev Biol broods on day 16 suggest that asynchronous hatching 56:253±277 substantially shortens the duration of high parental Drent RH, Klaassen M, Zwaan B (1992) Predictive growth budgets energy expenditure in parrotlets. Nevertheless, a link in terns and gulls. Ardea 80:5±17 Forshaw JM (1989) Parrots of the world, 3rd edn. Landsdowne, between such a reduction and reduced reproductive Willoughby, Australia costs still remains to be established. Stoleson and Be- Fujioka M (1985) Food delivery and sibling competition in ex- issinger (1997) were unable to detect dierences in perimentally even-aged broods of the cattle egret. Behav Ecol survival or future reproductive eorts of parents raising Sociobiol 17:67±74 Hahn DC (1981) Asynchronous hatching in the laughing gull: synchronous versus asynchronous broods, but they cutting losses and reducing rivalry. Anim Behav 29:421±427 cautioned that sample sizes were relatively small and HeÂ bert PN, Barclay RMR (1986) Asynchronous and synchronous statistical power to detect dierences was fairly low. hatching: eect on early growth and survivorship of herring One possibility inviting further study is that reduced gull, Larus argentatus, chicks. Can J Zool 64:2357±2362 Hussell DJT (1972) Factors aecting clutch size in Arctic passer- parental energy expenditure and/or reproductive costs ines. EcolMonogr 42:317±364 due to a shortened peak load may be oset by costs Lessells CM, Avery MI (1989) Hatching asynchrony in European associated with a longer overall period of parental care bee-eaters Merops apiaster. J Anim Ecol 58:815±835 (Fig. 2). Alternatively, green-rumped parrotlets have Lifson N, McClintock R (1966) Theory of use of the turnover rates unusually low ratios of FMR to basal metabolic rate, of body water for measuring energy and material balance. J Theor Biol 12:47±74 even during the days of peak brood energy demand Magrath RD (1990) Hatching asynchrony in altricial birds. Biol (R.B. Siegel, W.W. Weathers, S.R. Beissinger, unpub- Rev 65:587±622 lished data), suggesting that reproductive output in this McCarty JP (1996) The energetic cost of begging in nestling pas- species may not be energy limited at all. If breeding serines. Auk 113:178±188 Mock DW, Ploger BJ (1987) Parental manipulations of optimal parrotlets work well below physiological capacity hatch asynchrony in cattle egrets: an experimental study. Anim throughout the reproductive cycle, then the subtle Behav 35:150±160 changes in patterns of energy expenditure caused by Mock DW, Schwagmeyer PL (1990) The peak load reduction hatching asynchrony may not have any ®tness conse- hypothesis for avian hatching asynchrony. Evol Ecol 4:249± quences. Further work is needed to test the link between 260 Nagy KA (1980) CO2 production in animals: analysis of potential short-term energy costs and long-term reproductive errors in the doubly labeled water method. Am J Physiol success, and to explore the mechanisms that may relate 238:R466±R473 the two. Nagy KA (1983) The doubly labeled water (3HH18O) method: a guide to its use. Publication number 12-1417. University of California, Los Angeles Acknowledgements We thank Scott Stoleson for sharing unpub- O'Connell M (1989) Population dynamics of Neotropical small lished nestling growth data, and ThomaÂ s Blohm for allowing us to mammals in seasonal habitats. J Mammal 70:532±548 live and work on his ranch. Alan Krakauer assisted with ®eld- SAS (1988) SAS/STAT user's guide, release 6.03 edition. SAS In- work, and Carlos Bosque and Maria Andreina Pacheco provided stitute, Cary, NC logistic help and hospitality in Venezuela. Tom Famula assisted Siegel RB, Weathers WW, Beissinger SR (in press) Assessing pa- with SAS, and Walt Koenig and Mark Chappell provided helpful rental eort in a Neotropical parrot: a comparison of methods. comments on the manuscript. This research was supported by Anim Behav NSF Doctoral Dissertation Improvement Grant no. IBN-95- Slagsvold T (1997) Is there a sexual con¯ict over hatching asyn- 20846 to R.B.S. and W.W.W. and grants from the NSF (IBN 94- chrony in American robins? Auk 114:593±600 07349 and DEB-95-03194) and the National Geographic Society Stamps J, Clark A, Arrowood P, Kus B (1985) Parent-ospring to S.R.B. con¯ict in budgerigars. Behavior 94:1±40 Stoleson SH, Beissinger SR (1995) Hatching asynchrony and the onset of incubation in birds, revisited: when is the critical period? In: Power MD (ed) Current ornithology. Plenum, New References York, pp 190±270 Stoleson SH, Beissinger SR (1997) Hatching asynchrony, brood reduction, and food limitation in a Neotropical parrot. Ecol Amundsen T, Slagsvold T (1991) Asynchronous hatching in the Monogr 67:131±154 pied ¯ycatcher: an experiment. Ecology 72:797±804 Troth RG (1979) Vegetational types on a ranch in the central llanos Beissinger SR, Bucher EH (1992) Sustainable harvesting of of Venezuela. In: Eisenberg JF (ed) Vertebrate ecology in the parrots for conservation. In: Beissinger SR, Snyder NFR (eds) northern Neotropics. Smithsonian Institution Press, Washing- New World parrots in crisis: solutions from conservation ton, DC, pp 17±30 biology. Smithsonian Institution Press, Washington, DC, Waltman JR, Beissinger SR (1992) Breeding behavior of the green- pp 73±115 rumped parrotlet. Wilson Bull 104:65±84 Beissinger SR, Waltman JR (1991) Extraordinary clutch size and Weathers WW (1996) Energetics of postnatal growth. In: Carey C hatching asynchrony of a Neotropical parrot. Auk 108:863± (ed) Avian energetics and nutritional ecology. Chapman & Hall, 871 New York, pp 461±496 Bryant DM (1988) Energy expenditure and body mass changes as Weathers WW, Siegel RB (1995) Body size establishes the measures of reproductive costs in birds. Funct Ecol 2:23±34 scaling of postnatal metabolic rate: an interspeci®c analysis Bryant DM, Gardiner A (1979) Energetics of growth in house using phylogenetically independent contrasts. Ibis 127:532± martins (Delichon urbica). J Zool 189:275±304 543 450

Webster MD, Weathers WW (1989) Validation of single-sample Wood RA, Nagy KA, MacDonald S, Wakakuwa ST, Beckman RJ, doubly labeled water method. Am J Physiol 256:R572±R576 Kaaz H (1975) Determination of oxygen-18 in water contained Wiebe KL, Bortoletti GR (1994) Energetic eciency of reproduc- in biological samples by charged particle activation. Anal Chem tion: the bene®ts of asynchronous hatching for American kes- 47:646±650 trels. J Anim Ecol 63:551±560 Wilkinson L (1990) SYSTAT: the system for statistics. Systat, Evanston, Ill Communicated by W.A. Searcy